Social scene perception in autism spectrum disorder: An eye-tracking and pupillometric study

ABSTRACT Typically, developing humans innately place subjective value on social information and orient attention to it. This can be shown through tracking of gaze patterns and pupil size, the latter of which taps into an individual’s cognitive engagement and affective arousal. People with Autism Spectrum Disorder (ASD) present with atypical social, communicative and behavioral patterns, but underlying substrates of these behavioral differences remain unclear. Moreover, due to high comorbidity with other neurodevelopmental disorders, it is often difficult to distinguish which differences are distinctive to ASD. In this study, a group of 35 adolescents and young adults with neurodevelopmental disorders were tested to investigate the processing of social and non-social scenes in individuals who meet the diagnostic criteria for autism and those who do not. Eye tracking and pupillometry measures were collected while participants observed images of tightly controlled natural scenes with or without a human being. Contrary to individuals without autism diagnosis, participants with autism did not show greater pupillary response to images with a human. Participants with autism were slower to fixate on social elements in the social scenes, and this latency metric correlated with clinical measures of poor social functioning. The results confirm the clinical relevance of eye-tracking and pupillometric indices in the field of ASD. We discuss the clinical implications of the results and propose that analysis of changes in visual attention and physiological level to social stimuli might be an integral part of a neurodevelopmental assessment.

[1]  D. Wechsler Wechsler Intelligence Scale for Children , 2020, Definitions.

[2]  B. Laeng,et al.  Pupillometry , 2020, Definitions.

[3]  O. Pascalis,et al.  Infants rapidly detect human faces in complex naturalistic visual scenes. , 2019, Developmental science.

[4]  Taylor R. Hayes,et al.  Scan patterns during scene viewing predict individual differences in clinical traits in a normative sample , 2018, PloS one.

[5]  T. Donovan,et al.  The Human Fetus Preferentially Engages with Face-like Visual Stimuli , 2018, Current Biology.

[6]  Nicole R. Zürcher,et al.  Bumetanide for autism: more eye contact, less amygdala activation , 2018, Scientific Reports.

[7]  S. Mathôt Pupillometry: Psychology, Physiology, and Function , 2018, Journal of cognition.

[8]  C. Freitag,et al.  The locus coeruleus–norepinephrine system as pacemaker of attention – a developmental mechanism of derailed attentional function in autism spectrum disorder , 2018, The European journal of neuroscience.

[9]  Nicole R. Zürcher,et al.  Hypersensitivity to low intensity fearful faces in autism when fixation is constrained to the eyes , 2017, Human brain mapping.

[10]  A. Klin,et al.  Infant viewing of social scenes is under genetic control and atypical in autism , 2017, Nature.

[11]  Nicole R. Zürcher,et al.  Look me in the eyes: constraining gaze in the eye-region provokes abnormally high subcortical activation in autism , 2017, Scientific Reports.

[12]  T. Banaschewski,et al.  Validation of the Movie for the Assessment of Social Cognition in Adolescents with ASD: Fixation Duration and Pupil Dilation as Predictors of Performance , 2016, Journal of autism and developmental disorders.

[13]  Giles M. Anderson,et al.  Visual preference for social stimuli in individuals with autism or neurodevelopmental disorders: an eye-tracking study , 2016, Molecular Autism.

[14]  C. Nelson,et al.  Greater Pupil Size in Response to Emotional Faces as an Early Marker of Social-Communicative Difficulties in Infants at High Risk for Autism. , 2016, Infancy : the official journal of the International Society on Infant Studies.

[15]  Lam Son Nguyen,et al.  Profiling olfactory stem cells from living patients identifies miRNAs relevant for autism pathophysiology , 2016, Molecular Autism.

[16]  Gustaf Gredebäck,et al.  The TimeStudio Project: An open source scientific workflow system for the behavioral and brain sciences , 2015, Behavior Research Methods.

[17]  Taylor R. Hayes,et al.  Mapping and correcting the influence of gaze position on pupil size measurements , 2015, Behavior Research Methods.

[18]  B. Rogé,et al.  Visual social attention in autism spectrum disorder: Insights from eye tracking studies , 2014, Neuroscience & Biobehavioral Reviews.

[19]  Dima Amso,et al.  An Eye Tracking Investigation of Developmental Change in Bottom-up Attention Orienting to Faces in Cluttered Natural Scenes , 2014, PloS one.

[20]  G. Siegle,et al.  Pupillary Motility: Bringing Neuroscience to the Psychiatry Clinic of the Future , 2013, Current Neurology and Neuroscience Reports.

[21]  E. Walker,et al.  Diagnostic and Statistical Manual of Mental Disorders , 2013 .

[22]  Linda R. Watson,et al.  Hyporesponsiveness to social and nonsocial sensory stimuli in children with autism, children with developmental delays, and typically developing children , 2013, Development and Psychopathology.

[23]  Sylvain Sirois,et al.  Pupil diameter measurement errors as a function of gaze direction in corneal reflection eyetrackers , 2013, Behavior research methods.

[24]  Katarzyna Chawarska,et al.  Context modulates attention to social scenes in toddlers with autism. , 2012, Journal of child psychology and psychiatry, and allied disciplines.

[25]  R. Schultz,et al.  The social motivation theory of autism , 2012, Trends in Cognitive Sciences.

[26]  J. Martineau,et al.  Can pupil size and pupil responses during visual scanning contribute to the diagnosis of autism spectrum disorder in children? , 2011, Journal of psychiatric research.

[27]  F. Hutzler,et al.  Systematic influence of gaze position on pupil size measurement: analysis and correction , 2011, Behavior research methods.

[28]  Christopher Gillberg,et al.  The ESSENCE in child psychiatry: Early Symptomatic Syndromes Eliciting Neurodevelopmental Clinical Examinations. , 2010, Research in developmental disabilities.

[29]  P. Chapman,et al.  Do Gaze Cues in Complex Scenes Capture and Direct the Attention of High Functioning Adolescents with ASD? Evidence from Eye-tracking , 2010, Journal of autism and developmental disorders.

[30]  A. Kingstone,et al.  Saliency does not account for fixations to eyes within social scenes , 2009, Vision Research.

[31]  Mark H. Johnson,et al.  Atypical eye contact in autism: Models, mechanisms and development , 2009, Neuroscience & Biobehavioral Reviews.

[32]  Michael C. Frank,et al.  Eye-movements reveal attention to social information in autism spectrum disorder , 2009, Neuropsychologia.

[33]  P. Hancock,et al.  Viewing it differently: Social scene perception in Williams syndrome and Autism , 2008, Neuropsychologia.

[34]  M. Bradley,et al.  The pupil as a measure of emotional arousal and autonomic activation. , 2008, Psychophysiology.

[35]  John Colombo,et al.  Visual Scanning and Pupillary Responses in Young Children with Autism Spectrum Disorder , 2006, Journal of clinical and experimental neuropsychology.

[36]  G. Aston-Jones,et al.  Activation of monkey locus coeruleus neurons varies with difficulty and performance in a target detection task. , 2004, Journal of neurophysiology.

[37]  F. Volkmar,et al.  Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. , 2002, Archives of general psychiatry.

[38]  J. Mattingley,et al.  Neuroscience and Biobehavioral Reviews , 2002, Physiology & Behavior.

[39]  N. Ikegami,et al.  The actual process of rating the global assessment of functioning scale. , 2001, Comprehensive psychiatry.

[40]  H. Fitzgerald Autonomic pupillary reflex activity during early infancy and its relation to social and nonsocial visual stimuli. , 1968, Journal of experimental child psychology.

[41]  C Ounsted,et al.  The biological significance of gaze aversion with particular reference to the syndrome of infantile autism. , 1966, Behavioral science.

[42]  L. Kanner,et al.  Early infantile autism. , 1944, Pediatric clinics of North America.

[43]  D. Wechsler Wechsler Adult Intelligence Scale , 2021, Encyclopedia of Evolutionary Psychological Science.

[44]  Warren Jones,et al.  Mechanisms of Diminished Attention to Eyes in Autism. , 2017, The American journal of psychiatry.

[45]  Meia Chita-Tegmark,et al.  Social attention in ASD: A review and meta-analysis of eye-tracking studies. , 2016, Research in developmental disabilities.

[46]  R. Adolphs,et al.  The social brain: neural basis of social knowledge. , 2009, Annual review of psychology.

[47]  C. Gillberg,et al.  The FTF (Five to Fifteen): the development of a parent questionnaire for the assessment of ADHD and comorbid conditions , 2004, European Child & Adolescent Psychiatry.